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What Pneumaticity Tells Us About 'Prosauropods'

What Pneumaticity Tells Us About 'Prosauropods'

[Special Papers in Palaeontology 77, 2007, pp. 207–222]

WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’, AND VICE VERSA by MATHEW WEDEL University of California Museum of and Department of Integrative Biology, 1101 Valley Life Sciences Building, Berkeley, CA 94720-4780, USA; e-mail: [email protected]

Typescript received 15 February 2006; accepted in revised form 24 October 2006

Abstract: Pneumatic (air-filled) are an important fea- may have evolved once (at the base of Ornithodira), twice ture of the postcranial skeleton in , theropods and (independently in pterosaurs and saurischians) or three times sauropods. However, there is no unambiguous evidence for (independently in pterosaurs, theropods and sauropods). Skel- postcranial pneumaticity in sauropodomorphs and even etal pneumaticity appears to be more evolutionarily malleable the ambiguous evidence is scant. Patterns of skeletal pneumati- than the air sacs and diverticula that produce it. The zation in early sauropods and theropods suggest that basal sau- of air sacs probably pre-dated the appearance of skeletal pneu- rischians had cervical air sacs like those of . Furthermore, maticity in ornithodirans. patterns of pneumaticity in most pterosaurs, theropods and sauropods are diagnostic for abdominal air sacs. The air sacs Key words: Prosauropoda, , , necessary for flow-through ventilation like that of birds Ornithodira, pneumaticity, air sacs, diverticula.

Pneumaticity is a prominent feature of the postcra- However, the or of the group of nial skeleton in theropod and sauropod . In con- taxa traditionally called prosauropods is not critical to the trast, there is little evidence for postcranial pneumaticity in purposes of this paper. What is important is that all tra- basal sauropodomorphs (informally referred to as ‘prosaur- ditional ‘prosauropods’ have two things in common: they opods’ in this paper), although from time to time some lack unequivocal evidence of pneumatic cavities in their aspects of prosauropod osteology have been posited as evi- vertebrae and ribs, and they are phylogenetically brack- dence of pneumaticity (Britt 1997) or compared with eted by sauropods and theropods (Text-fig. 1). unequivocal pneumatic structures in sauropods (Yates 2003; Galton and Upchurch 2004). My goals in this paper Institutional abbreviations. BMNH, The Natural History are to review the evidence for postcranial skeletal pneuma- Museum, London; CM, Carnegie Museum of Natural His- ticity (PSP) in prosauropods and to discuss the origin of air tory, Pittsburgh, USA; FMNH, Field Museum of Natural History, sacs and pneumaticity in early dinosaurs and their relatives. Chicago, USA; MSM, Mesa Southwest Museum, Mesa, USA; Prosauropod is currently in a state of flux, OMNH, Oklahoma Museum of Natural History, Norman, USA; SMNS, Staatliches Museum fur Natu¨rkunde, Stuttgart, Germany. as other papers in this volume attest (Sereno 2007; Upchurch et al. 2007; Yates 2007). Prosauropods were Anatomical abbreviations. ACDL, anterior centrodiapophyseal traditionally considered a paraphyletic assemblage that lamina; AL, accessory lamina; AVF, anteroventral fossa; NAF, gave rise to sauropods. Sereno (1998) recovered a mono- neural arch fossa; PCDL, posterior centrodiapophyseal lamina; phyletic Prosauropoda, defined this (anchored upon PDF, posterodorsal fossa; PODL, postzygodiapophyseal lamina; ) as a monophyletic sister to PPDL, paradiapophyseal lamina; PRDL, prezygodiapophyseal and united the two in a node-based Sauropodomorpha. A lamina; SPOL, spinopostzygapophyseal lamina; SPRL, spinoprezy- similar phylogenetic hypothesis was described by Galton gapophyseal lamina (lamina abbreviations after Wilson 1999). and Upchurch (2004). However, other recent phylogenet- ic analyses (Yates 2003, 2004; Yates and Kitching 2003) have found that some prosauropods are closer to Salta- POSTCRANIAL PNEUMATICITY IN saurus than to Plateosaurus; thus, under current phylo- THEROPOD AND SAUROPOD genetic definitions they should be regarded as basal DINOSAURS sauropods. Some other taxa (e.g. Saturnalia) lie outside Sauropodomorpha as defined by Sereno (1998) altogether Before examining the evidence for PSP in ‘prosauropods’, (Yates 2003, 2004; Yates and Kitching 2003; Langer 2004). I will review the conditions present in other saurischian

ª The Palaeontological Association 207 208 SPECIAL PAPERS IN PALAEONTOLOGY, 77

skin. Where a diverticulum comes into contact with a , it may (but does not always) induce bone resorp- tion, which can produce pneumatic tracks, fossae or for- amina. If resorption of the cortex produces a foramen, the diverticulum may enter the medullary space and replace the existing internal structure with a series of air- filled chambers of varying complexity. The best descrip- tion of this process is provided by Bremer (1940). The extent of PSP varies in different avian . Almost any postcranial bones can become pneumatized; in large soaring birds such as pelicans, almost the entire skeleton is pneumatic, including the distal elements (O’Connor 2004). Although many large volant and flight- less birds have highly pneumatic skeletons, the correlation between body size and the extent of PSP in birds is weak (O’Connor 2004). PSP tends to be reduced or absent in diving birds (Gier 1952; O’Connor 2004). Different parts of the skeleton become pneumatized by diverticula of dif- ferent air sacs in extant birds (Table 1); this is important because it allows us to make inferences regarding the evo- lution of air sacs in fossil taxa. PSP in non-avian thero- TEXT-FIG. 1. A phylogeny of showing the pods generally follows the avian model (Britt 1993, 1997; evolution of postcranial skeletal pneumaticity and air sacs. O’Connor and Claessens 2005; O’Connor 2006). Patterns is shown as having limited postcranial of pneumatization along the indicate pneumaticity. The evidence for this is ambiguous; see text for that both anterior and posterior air sacs (presumably cer- discussion. Based on the phylogenetic framework of Brochu vical and abdominal) had evolved by the time of the cer- (2001) and Yates (2003). atosaur-tetanuran divergence (O’Connor and Claessens 2005). dinosaurs. The sister taxon of Sauropodomorpha is Ther- Fossae are present in the presacral vertebrae of basal opoda; consequently, ‘prosauropods’ are phylogenetically sauropods such as and (Britt bracketed in part by birds, the only clade of extant verte- 1993; Wilson and Sereno 1998). These fossae are similar brates with extensive PSP. The relationship between the to the unequivocally pneumatic foramina and camerae of respiratory system and pneumatic postcranial bones in more derived sauropods, both in their position on indi- birds has been described many times (e.g. Mu¨ller 1908; vidual vertebrae and in their distribution along the ver- King 1966; Duncker 1971; O’Connor 2004), and is briefly tebral column, and because of these similarities they have summarized here. The relatively small, constant-volume, usually been regarded as pneumatic in origin (Britt 1993, unidirectional flow-through of birds are ventilated 1997; Wedel 2003a). However, similar fossae are present by the attached air sacs, which are large, flexible and in other that lack PSP, so the presence of fossae devoid of parenchymal tissue. The lungs and air sacs also alone is at best equivocal evidence for PSP (O’Connor produce air-filled tubes called diverticula that pass 2006; see below). The vertebrae of more derived sauro- between the viscera, between the muscles, and under the pods have foramina that communicate with large internal

TABLE 1. Parts of the postcranial skeleton that are pneumatized by diverticula of different parts of the respiratory system in extant birds. Pneumaticity varies widely within populations and clades, and not all elements are pneumatized in all taxa (based on Duncker 1971 and O’Connor 2004).

Respiratory structure Skeletal elements

Lung (parenchymal portion) Adjacent thoracic vertebrae and ribs Clavicular Sternum, sternal ribs, pectoral girdle and humerus Cervical air sac Cervical and anterior thoracic vertebrae and associated ribs Anterior thoracic air sac Sternal ribs Posterior thoracic air sac (none reported) Abdominal air sac Posterior thoracic, synsacral and caudal vertebrae, pelvic girdle and Subcutaneous diverticula Distal limb elements WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 209 chambers; the combination of foramina and large internal shown that the ilial chambers are connected to foramina, chambers is an unambiguous indicator of PSP (O’Connor which are necessary for pneumatization to occur (see 2006). There is a general trend in sauropod evolution for O’Connor 2006). PSP to spread posteriorly along the vertebral column, albeit to different extents in different clades and with a few reversals (Wedel 2003b; Text-fig. 2). In both sauro- EVIDENCE OF PNEUMATICITY IN pods and theropods, fossae in basal forms were replaced ‘PROSAUROPODS’ by large-chambered (camerate) vertebrae and eventually small-chambered (camellate) vertebrae in more derived Historically, postcranial pneumaticity in ‘prosauropods’ taxa (Britt 1993, 1997; Wedel 2003a). has received little attention, which is to be expected given The evolution of PSP in sauropods mirrors in detail the paucity of available evidence. Janensch (1947) posited that of non-avian theropods. At the level of individual that a foramen in a dorsal of Plateosaurus might elements (e.g. vertebrae and ribs), pneumatic features in have been pneumatic, but he attached no great weight to sauropods compare very closely with those of both avian this hypothesis. Britt (1997) considered vertebral laminae and non-avian theropods (Text-fig. 3). In terms of the evidence of pneumaticity in ‘prosauropods’. Most ratio of bony tissue to air space within a pneumatic ele- recently, Yates (2003, p. 14, fig. 12) identified ‘pleurocoel- ment, sauropod vertebrae are, on average, comparable like pits’ in the mid- of Thecodontosau- with the limb bones of many extant birds: about 60 per rus caducus, and Galton and Upchurch (2004, p. 245) cent air by volume (Wedel 2004, 2005; Woodward 2005; referred to fossae in the posterior dorsals of some pro- Schwarz and Fritsch 2006). At the level of the skeleton, sauropods as ‘pleurocoelar indentations’. The ‘pleurocoel- osteological indicators of pneumaticity spread as far back like’ structures were not explicitly described as pneumatic as the mid-caudal vertebrae in at least two groups of in either work. Although fossae are not unambiguous sauropods, the diplodocines and saltasaurines (Osborn indicators of pneumaticity (O’Connor 2006), vertebral 1899; Powell 1992). Among non-avian theropods, exten- fossae seem to be an early step toward full pneumatiza- sive pneumatization of the caudal series evolved only in tion, both ontogenetically and phylogenetically (Wedel oviraptorosaurs (Osmo´lska et al. 2004). Finally, limited 2003a). Putative pneumatic characters in ‘prosauropods’ appendicular pneumaticity was probably present in both can be divided into three categories: vertebral laminae, sauropods and non-avian theropods. The dromaeosaur foramina and fossae, which will be discussed in this Buitreraptor has a pneumatic furcula (Makovicky et al. , below. 2005), and a large foramen in the proximal femur of the oviraptorid Shixinggia is probably also pneumatic in ori- Vertebral laminae. Vertebral laminae are struts or plates of gin (Lu¨ and Zhang 2005). Large chambers have been bone that connect the various apophyses of a vertebra to reported in the ilia of the basal diplodocoid Amazonsau- each other and to the centrum. The landmarks that are rus (Carvalho et al. 2003) and in several titanosaurs usually connected in this way are the pre- and postzygapo- (Powell 1992; Sanz et al. 1999; Xu et al. 2006). Although physes, the diapophyses and parapophyses, and the neu- these chambers are similar to unequivocally pneumatic rapophysis. The form and occurrence of the major spaces in the other saurischians, it has not yet been laminae in saurischian dinosaurs were reviewed by Wilson

TEXT-FIG. 2. A diagram showing the distribution of fossae and pneumatic chambers (black boxes) along the vertebral column in sauropods. Only the lineage leading to diplodocines is shown here. The same caudal extension of pneumatic features also occurred independently in macronarian sauropods, culminating in saltasaurines, and several times in theropods. The format of the diagram is based on Wilson and Sereno (1998, fig. 47). Phylogeny based on Wilson (2002), Yates (2003) and Upchurch et al. (2004). 210 SPECIAL PAPERS IN PALAEONTOLOGY, 77

AB C TEXT-FIG. 3. Pneumatic foramina (black) in thoracic or dorsal vertebrae of an extant , a non-avian theropod and a sauropod, in right lateral view (above) and posterior view (below). A, a crane, Grus. B, an abelisaurid, Majungatholus. C, a diplodocid, . A and B traced from O’Connor and Claessens (2005, fig. 3); C traced from a photograph of OMNH 1382. Scale bars represent 1 cm in A, 3 cm in B and 20 cm in C.

(1999). In addition to a basic set of laminae common to The second question can be stated: do laminae grow all saurischians, many sauropods and theropods have other out from the corpus of the vertebra to define the fossae irregularly developed laminae that are usually not named that they bound, or do we only recognize laminae as dis- but are collectively called accessory laminae. Laminae tend tinct structures because the bone between them has been to be more numerous and more sharply defined in camer- removed? For example, the cervical vertebra of Nigersau- ate than camellate vertebrae (Wilson and Sereno 1998; rus illustrated by Sereno and Wilson (2005, fig. 5.8) has Wedel 2003a). Camellate vertebrae evolved relatively early on the lateral face of the neural spine two fossae divided in the radiation of non-avian theropods (Britt 1993, 1997), by an accessory lamina (Text-fig. 4). At its edges, the and most derived theropods have less elaborate systems of anteroventral fossa approaches both the prezygapophysis laminae than neosauropods. This may explain why the lit- and the diapophysis. This region is flat or convex in most erature on laminae has tended to focus on sauropods (e.g. other neosauropods, which have a lateral fossa in roughly Osborn 1899; Osborn and Mook 1921; Janensch 1929, the same position as the posterodorsal fossa in Nigersau- 1950; Wilson 1999). rus. It seems likely therefore that the anteroventral fossa Two problems with the identification of laminae that in is a new morphological feature, and that are relevant to the question of pneumaticity are how well the accessory lamina can only be recognized as a lamina developed a ridge of bone must be before we call it a because a fossa has been excavated below it. Conversely, lamina, and whether laminae are primarily additive struc- the vertebrae of most tetrapods do not have straight bars tures formed by the deposition of new bone, or are sim- of bone that connect the zygapophyses to the neurapoph- ply bone that is left over following the formation of ysis, but this is exactly what the spinopre- and fossae. The first problem is important because, as shown spinopostzygapophyseal laminae of some sauropods do below, incipient laminae are broadly distributed among (Text-fig. 4). In comparison with the condition in other archosaurs. To what extent are the distinct laminae of tetrapods, including prosauropods, these laminae appear saurischian dinosaurs new (¼ apomorphic) structures, to be additive structures. These potentially opposing pro- rather than modifications of pre-existing ones? This ques- cesses of lamina formation should be kept in mind while tion has ramifications for the evolution of laminae reading the following descriptions. and for coding of laminae as characters in phylogenetic The laminae of sauropods often form the boundaries of analyses. fossae that have been interpreted as pneumatic, either WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 211

TEXT-FIG. 4. Laminae, fossae and foramina in cervical vertebrae of Nigersaurus and Apatosaurus. A, fifth cervical vertebra of Nigersaurus, traced from Sereno and Wilson (2005, fig. 5.8). B, tenth cervical vertebra of Apatosaurus, traced from Gilmore (1936, pl. 24). Scale bars represent 5 cm in A and 20 cm in B.

because they contain foramina that lead to internal cham- The laminae of ‘prosauropods’ differ from those of bers or because they are heavily sculpted, with numerous sauropods in three important ways. The first is that pro- subfossae (sensu Wilson 1999) and a distinct bony texture sauropods have fewer laminae. The laminae that connect (although texture alone is not necessarily a good indicator the diapophysis to the centrum, parapophysis and zygap- of pneumaticity; see O’Connor 2006). Wilson (1999) con- ophyses are usually present (Wilson 1999), but those that sidered whether sauropod laminae existed to provide connect the neurapophysis to other landmarks are absent mechanical support or to subdivide pneumatic diverti- (Text-fig. 5; but see Bonaparte 1999, figs 13–16 on Les- cula, and concluded that they probably served both func- semsaurus). The second is that laminae are confined to tions simultaneously. Following from the aforementioned the presacral vertebrae in ‘prosauropods’, whereas the sac- discussion, we might also ask if sauropod laminae exist ral vertebrae of neosauropods and the caudal vertebrae of because the pneumatic diverticula are subdivided, as they diplodocids also bear laminae. often are in birds (e.g. Wedel 2003b, fig. 2), and these The third and most important difference between the subdivisions are impressed into the bone, leaving laminae laminae of sauropods and ‘prosauropods’ is that the fos- between them. Rather than try to determine which struc- sae bounded by the latter are blind. These fossae do not ture has morphogenetic precedence, it may be more use- contain foramina or subfossae and they do not have a ful to view sauropod vertebrae in light of Witmer’s distinctive bone texture. Consequently, there is no strong (1997) hypothesis that the form of a pneumatic bone can reason to suspect that they contained pneumatic diverti- be viewed as the outcome of a struggle between bone tis- cula. O’Connor (2006) found that similar fossae in extant sue, which grows partly in response to biomechanical crocodilians and birds may contain cartilage or adipose stress, and pneumatic diverticula, which are opportunistic tissue. Considering whether the laminae are additive and invasive and spread wherever possible (see Sadler structures or remnants of fossa formation sheds little light et al. 1996 and Anorbe et al. 2000 for examples of prolif- on the problem. Some laminae, such as the PRDLs of erating diverticula). Plateosaurus cervicals, are straight-line structures that

ABPODL PODL PRDL PRDL PCDL

PPDL

PCDL groove

TEXT-FIG. 5. Vertebrae of Plateosaurus trossingensis (SMNS 13200) in left lateral view. A, the eighth cervical vertebra. B, dorsal vertebrae 1–4. Scale bars represent 5 cm. 212 SPECIAL PAPERS IN PALAEONTOLOGY, 77 appear to have been added, compared with the condition On one hand, it is possible that the laminae and fossae in vertebrae that lack laminae (Text-fig. 5). Others, such of basal archosauriform and pseudosuchian vertebrae as the PODLs in the same vertebrae, are only detectable appear pneumatic because they are pneumatic (Gower because they have been undercut by a fossa. The form of 2001), but the morphology is not compelling. Like the the fossae themselves provides no obvious clues to their fossae of ‘prosauropod’ neural spines, those of Erythrosu- contents in vivo. chus and Arizonasaurus lack subfossae, foramina that lead Laminae like those of ‘prosauropods’ occur in many to large internal chambers, or altered texture. The pres- other archosaurs. Desojo et al. (2002) and Parker (2003) ence of similar features in crocodyliforms and salaman- recognized that many of the laminae described by Wilson ders is strong evidence that the morphologies in question (1999) for saurischian dinosaurs are also present in basal can be produced in the absence of pneumaticity. Unlike archosaurs and pseudosuchians. The full complement of ‘prosauropods’, basal archosauriforms and pseudosuchi- diapophyseal laminae is present in dorsal vertebrae of the ans are not bracketed by taxa with unequivocal evidence basal archosauriform Erythrosuchus and in those of popo- of pneumaticity, so inferring that they had pneumatic saurs such as Sillosuchus and Arizonasaurus, including the vertebrae would require pulmonary diverticula and poss- PCDL, PODL, PPDL and PRDL (Text-fig. 6; see Alcober ibly also air sacs to have evolved much earlier than other- and Parrish 1997; Nesbitt 2005). At least in Erythrosuchus, wise supposed (see ‘Palaeobiological implications’ below). the fossae bounded by these laminae contain aggregates Regardless of when the capacity for PSP evolved, the of vascular foramina; obvious foramina like these are not laminae of ‘prosauropods’ bound fossae that are not present or at least not common in the interlaminar fossae unequivocally pneumatic. Similar laminae are present in of ‘prosauropods’ (pers. obs.). Incipient laminae are also crocodilians, a group in which postcranial pneumaticity is present in some neosuchian crocodyliforms. Most dorsal entirely absent. Some of the osteological traces of diverti- vertebrae of Goniopholis stovalli have rudimentary PCDLs cula are subtle, and the possibility that the neural arch and PODLs (Text-fig. 7). The PODL is bounded dorsally fossae of ‘prosauropods’ accommodated pneumatic diver- by a shallow fossa on the lateral face of the neural spine ticula cannot be ruled out, but there is no strong evidence and ventrally by a deep infrapostzygapophyseal fossa. In for it. at least some of the vertebrae, the fossa on the side of the neural spine has a distinct margin (Text-fig. 7B). Foramina. The only putative pneumatic foramen in a Although most neosuchian crocodyliforms have extensive ‘prosauropod’ is that described by Janensch (1947) in a pneumatization (Witmer 1997; Tykoski et al. 2002), cervical vertebra of Plateosaurus. Janensch argued that the PSP is absent in the clade (O’Connor 2006). size (11 · 4 mm) and form of the foramen were more Vertebral laminae also occur in non-amniotes. The best consistent with a pneumatic than a vascular interpret- example is probably the plethodontid salamander Aneides ation. The identity of the foramen can only be settled by lugubris, in which plate-like shelves of bone connect the first-hand observation, preferably with a computed tomo- parapophyses of dorsal vertebrae to the ventrolateral mar- graphic (CT) scan to determine if the foramen leads to gins of the centra (Wake 1963). These shelves of bone are any large internal chambers. Unfortunately, such an absent in other species of Aneides and in other pletho- examination has yet to be conducted. However, the cau- dontid genera, and they are thus additive structures that dal vertebrae of some whales are similar in size to Plateo- are apomorphic for A. lugubris (compare Wake 1963, saurus dorsal vertebrae (c. 20 cm in maximum linear fig. 9 with Wake and Lawson 1973, fig. 6). A. lugubris has dimension) and have vascular foramina up to 30 mm in the most prolonged ontogeny of any plethodontid, and it diameter (pers. obs.), so large foramina do not necessarily is peramorphic relative to other species in the , with indicate the presence of pneumaticity. In general, the a more extensively ossified skeleton (Wake 1963; Wake prominent foramina and internal chambers that are typ- et al. 1983). The development of laminae in the species is ical of sauropod vertebrae are absent in the vertebrae of probably an epiphenomenon of the extensive ossification ‘prosauropods’. of the skeleton, which in turn is related to adaptations for arboreality and feeding (Larson et al. 1981). As such, the Fossae. The first step in recognizing pneumatic fossae is laminae of A. lugubris are not homologous with those of to distinguish between vertebrae that have distinct fossae archosaurs in a taxic sense, and they are probably pro- and those that are merely waisted (narrower in the mid- duced by different developmental processes. Still, A. lugu- dle than at the ends). The vertebrae of most vertebrates bris demonstrates that laminae can evolve in vertebrates are waisted to some extent. In humans the effect is barely that are far removed from basal dinosaurs in both gene- noticeable, but in some archosaurs the ‘waist’ of the ver- alogy and body size, and it provides a potential system in tebra may be only half the diameter of the ends of the which to investigate the development of laminae in an centrum (e.g. Nesbitt 2005, fig. 16). Some degree of extant . waisting is to be expected based on the early development WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 213

TEXT-FIG. 6. Dorsal vertebrae of A Erythrosuchus africanus (BMNH R533). A, right lateral and B, ventrolateral views. Scale bar represents 5 cm.

PODL PRDL

PPDL

PCDL

B

vascular foramina

of vertebrae. Cell-dense regions of the embryonic axial waisted but lacks distinct fossae: for example, a thoracic column become intervertebral discs, and lower-density vertebra of an artiodactyl. At the other end is a vertebra regions become vertebral bodies. This produces centra with large foramina that open into internal chambers, that are inherently waisted (Verbout 1985, pl. 10; Wake such as a dorsal vertebra of . The ‘chamber 1992, figs 6.5, 6.7). The degree of waisting has occasion- morphospace’ between these endpoints is filled with a ally been used as a taxonomic character (Case 1907), but continuum of deeper and more distinct fossae and cam- to date there is no clear explanation of why some verteb- erae. Adjacent to the artiodactyl vertebra we might put a rae are more waisted than others. Regardless, vertebral vertebra that has fossae with a distinct margin on one waisting is widespread in vertebrates and is not evidence side but not the other, like those in the cervical centra of for pneumaticity. Arizonasaurus, which are bounded dorsally by the PCDL; Waisting aside, fossae still suffer from a problem of next, a fossa that has a distinct bony rim on all sides, but definition. Consider a spectrum of morphological possi- that is not enclosed by a bony lip, like those in dorsal bilities (Text-fig. 8). At one end is a vertebra that is centra of adult Barapasaurus or juvenile Apatosaurus. The 214 SPECIAL PAPERS IN PALAEONTOLOGY, 77

TEXT-FIG. 7. Dorsal and caudal AB vertebrae of Goniopholis stovalli. These PODL vertebrae are part of an associated NAF collection of several individuals from the type locality of the species. A, a dorsal vertebra (OMNH 2504) in left posterolateral view. B, a dorsal vertebra (OMNH 2470) in right lateral view. C, a middle caudal centrum (OMNH 2448) incipient PODL in right lateral view. D, a distal caudal PCDL centrum (OMNH 2454) in left lateral view. White arrows in B and D highlight the margins of fossae. Scale bar represents 1 cm.

CD

fossa fossa

penultimate example is a fossa that is enclosed by a bony pneumatic foramina are usually located inside the cervical lip, but that is little expanded beyond the boundaries of rib loop or ansa costotransversaria). the opening, such as the fossae in presacral centra of The foregoing discussion implies that where chambers [Britt (1993) referred to these cham- lack a distinct lip of bone, geometry alone is a poor clue bers as camerae, whereas Wedel termed them fossae to whether or not a given fossa has a pneumatic origin. (Wedel et al. 2000; Wedel 2003a). The morphology of Other lines of evidence must be used, such as position in these features is intermediate between that of fossae and the body, the presence or absence of adjacent pneumatic camerae, and either term could reasonably be applied]. foramina, subfossae, or textural differences (and even the Finally, in neosauropods such as and Salta- last two may be misleading; see O’Connor 2006). saurus the space beyond the bony lip is greatly expanded, Vertebral centra of ‘prosauropods’ can be quite nar- so that the result is a foramen that leads to camerae or row-waisted, and some have lateral grooves or fossae that camellae. are bounded on one side by a lamina. As with neural arch The fossae along this spectrum vary in geometry and laminae, these features are sometimes associated with they are not all pneumatic. Although Goniopholis is pneumaticity but they are not diagnostic for it. The extinct and not part of the crown-group Crocodylia, it is ‘pleurocoelar indentations’ mentioned by Galton and highly unlikely that the caudal vertebrae of this semi- Upchurch (2004) do not have a distinct boundary or lip aquatic neosuchian were pneumatic. Nevertheless, they in any of the specimens that I have examined (e.g. Moser bear lateral fossae with distinct margins that are very sim- 2003, pl. 16). The only known ‘prosauropod’ with dis- ilar to structures that are sometimes interpreted as pneu- tinctly emarginated lateral fossae is Thecodontosaurus matic in dinosaurs, such as the sacral ‘pleurocoels’ of caducus (Yates 2003). Cervical vertebrae 6–8 of BMNH ornithomimosaurs. However, distinct margins alone are P24, the holotype of T. caducus, have small, distinct fos- not compelling evidence of pneumaticity. Conversely, sae just behind the diapophyses (Text-fig. 10). The fossae truly pneumatic fossae need not have distinct margins. are high on the centra and may have crossed the neuro- For example, the fossae behind the prezygapophyses of central sutures, which are open. The fossa on the eighth ratites lack clear margins, but CT scans show that they cervical looks darker than it should because it is coated house pneumatic diverticula, and they sometimes contain with glue. The ninth cervical has a very shallow, tear- pneumatic foramina (Text-fig. 9). In extant birds, the drop-shaped hollow in the same region of the centrum. pneumatic canalis intertransversarius lies alongside the The bone texture in this hollow is noticeably smoother centrum (Mu¨ller 1908), but many birds have cervical cen- than on the rest of the centrum (this is especially appar- tra that are laterally convex and lack any fossae (the ent under low-angle lighting). That the fossa on the ninth WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 215

TEXT-FIG. 8. Diagram showing the evolution of fossae and pneumatic chambers in sauropodomorphs and their outgroups. Vertebrae are shown in left lateral view with lines marking the position of the cross-sections, and are not to scale. The omission of ‘prosauropods’ from the figure is deliberate; they have no relevant apomorphic characters and their vertebrae tend to resemble those of many non-dinosaurian archosaurs. Cross-sections are based on first-hand observation (Giraffa and Arizonasaurus), published sections (Barapasaurus, Camarasaurus and Saltasaurus)orCT scans (Apatosaurus and Haplocanthosaurus). Giraffa based on FMNH 34426. Arizonasaurus based on MSM 4590 and Nesbitt (2005, fig. 17). Barapasaurus based on Jain et al. (1979, pls 101–102). Apatosaurus based on CM 11339. Haplocanthosaurus based on CM 572. Camarasaurus based on Ostrom and McIntosh (1966, pl. 24). Saltasaurus modified from Powell (1992, fig. 16).

cervical is shallower and less distinct than those on cervi- distinct margins of the fossae in cervicals 6–8, and also cals 6–8 is reminiscent of the diminution of pneumatic on the fact that the fossae only occur on cervicals 6–9 features observed at the transition from pneumatic to (Wedel 2006). The first line of evidence is inadequate to apneumatic vertebrae, as seen in the anterior dorsal ver- diagnose pneumaticity unequivocally. The second is also tebrae of (Sereno et al. 1999, fig. 3) and the mid- problematic. Cervical vertebrae 5–9 are the only ones that dle caudal vertebrae of (Osborn 1899, fig. 13). are always pneumatized in the chicken (Hogg 1984a), and The holotype specimen of T. caducus represents an imma- the cervical and anterior thoracic vertebrae are the first ture individual (Yates 2003), however, so the shallow parts of the axial skeleton to be pneumatized during the fossa on the ninth cervical may be incompletely devel- ontogeny of birds (Cover 1953; Hogg 1984b). The spread oped. of pneumaticity posteriorly along the vertebral column in Are the fossae of T. caducus pneumatic? If so, they are the ontogeny of birds appears faithfully to recapitulate the only good evidence for invasive pneumatic features in the evolution of pneumaticity in theropods and sauro- the of ‘prosauropods’. Previously, I have pods (Wedel 2003b, 2005). The presence of fossae on the assumed that they were pneumatic, based in part on the midcervical vertebrae of T. caducus is easily explained if 216 SPECIAL PAPERS IN PALAEONTOLOGY, 77

the best evidence for potential pneumaticity in ‘prosauro- pods’, but neither is an unambiguous indicator of PSP and both would benefit from further study. In any case, the diagnostic osteological correlatives of pneumaticity that are common in sauropods and theropods are absent or extremely rare in ‘prosauropods’, and the putative pneumatic features that are widespread in ‘prosauropods’ (laminae and shallow fossae) are not compelling evidence pneumatic pneumatic of pneumaticity. To leave aside for a moment the ques- foramen fossa tion of ‘prosauropod’ monophyly, ‘prosauropods’ are unusual as the only sizeable group (or grade) of saurischi- an dinosaurs that lack extensive PSP.

PALAEOBIOLOGICAL IMPLICATIONS

Pneumatic bones are of palaeobiological interest in two ways. We may be interested in the bones themselves: in their external and internal morphology, in the ratio of bone to air space, and in the ways that they develop. They are also important, arguably more important, as osteological markers of the pulmonary system. In this sec- tion I discuss the origins of pneumaticity and of air sacs, and the implications for the respiratory physiology of TEXT-FIG. 9. An uncatalogued cervical vertebra of an emu sauropodomorphs. (Dromaius novaehollandiae) from the OMNH comparative collection. Scale bar represents 2 cm. Origin of the diverticular lung and PSP. The first part of the postcranial skeleton to be pneumatized in any sauris- the fossae are pneumatic; their appearance in that part of chian is the cervical column. The fossae in the the skeleton mirrors early ontogeny in birds and is also mid-cervical vertebrae of Thecodontosaurus caducus are consistent with later trends in the evolution of PSP in not definitely pneumatic on the basis of geometry alone. sauropodomorphs (Text-fig. 2). On all four vertebrae, the However, their placement in the skeleton is suspiciously fossae are not closely associated with laminae and cannot similar to the early stages of pneumatization in birds. The be dismissed as epiphenomena of lamina formation (see same is true of fossae in the cervical column of the basal O’Connor 2006); a specific soft-tissue influence was caus- sauropod Shunosaurus (Wilson and Sereno 1998). Among ally related to the formation of the fossae. The geometry basal theropods, Coelophysis bauri is the earliest well-rep- of the fossae is not sufficient to specify that soft-tissue resented taxon with evidence of pneumaticity. The post- influence because adipose, muscular and pulmonary tis- axial cervical vertebrae of C. bauri have pneumatic sues have all been found to occupy similar fossae in other cavities that occupy most of the neural spine and that tetrapods (O’Connor 2006). On the other hand, the pres- communicate with the outside through several large for- ence of the fossae only on the midcervical vertebrae is dif- amina (Colbert 1989). ficult to explain if they were not produced by pneumatic The pattern of pneumatization in these early diverging diverticula like those of more derived sauropods. saurischians indicates the presence of cervical air sacs like those of birds. It is true that in sauropsids diverticula Summary. Vertebral laminae and shallow depressions on may develop from practically any portion of the respirat- the centra are widespread in archosauriforms and not ory system. However, it does not follow that the diverti- diagnostic of pneumaticity, although it is difficult to rule cula that pneumatize the skeleton can come from out the possibility that they may have been associated anywhere (contra Hillenius and Ruben 2004), for two rea- with pneumatic diverticula. ‘Prosauropods’ have fewer sons. First, in extant birds the cervical vertebrae are only laminae than most sauropods, fewer vertebrae with lam- pneumatized by diverticula of cervical air sacs. Diverticula inae, and the fossae adjacent to the laminae are almost of the cranial air spaces, larynx and trachea are never always blind (with no large foramina or chambers). A known to pneumatize the postcranial skeleton (King foramen in a vertebra of Plateosaurus and distinct fossae 1966), and diverticula of the parenchymal portion of the in the cervical vertebrae of Thecodontosaurus caducus are lung only pneumatize the vertebrae and ribs adjacent to WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 217

A

B

TEXT-FIG. 10. Vertebrae of Thecodontosaurus caducus, BMNH P24. A, cervical vertebrae 6–8 in left lateral view. B, cervical vertebra 9 in right lateral view. Scale bars represent 1 cm. the lungs (O’Connor 2004). Second, as discussed below, Furthermore, diverticula did not evolve to pneumatize pneumatization of the posterior half of the body is the skeleton. In the first place, many of the diverticula of accomplished only by diverticula of abdominal air sacs birds are visceral, subcutaneous or intermuscular, and do (O’Connor and Claessens 2005). These observations of not pneumatize any bones (Duncker 1971). Skeletal extant taxa provide valuable guidelines for interpreting pneumatization cannot be invoked to explain the pres- patterns of skeletal pneumatization in fossil taxa. ence of these diverticula. In the second place, the presence Pneumatization by diverticula of cervical air sacs is the of diverticula is a prerequisite for pneumatization of the only mechanism for pneumatizing the that is (1) skeleton. The immediate ancestors of Coelophysis and known to occur in extant taxa and (2) consistent with the Thecodontosaurus must have already had cervical diverti- pattern of pneumatization found in basal saurischians cula (assuming that the fossae of the latter are pneumatic (Wedel 2006). in origin). Pneumatization of the cervical series could not Pneumaticity in basal saurischians is extremely limited. happen until these diverticula were already in place, so The bone removed by pneumatization of the postcranial the diverticula must have evolved for some other reason. skeleton (or fossa formation, if the fossae of Thecodonto- Alternatively, the origins of paravertebral diverticula saurus are not pneumatic) accounted for much less than and of PSP may have been coincident. The first step may 1 per cent of the total body volume in both Coelophysis have been a developmental accident that allowed the and Thecodontosaurus (see Appendix), compared with diverticula to push beyond the coelom and these several per cent for more derived sauropods and thero- ‘unleashed’ diverticula may have pneumatized the verteb- pods (Wedel 2004, 2005). PSP probably did not evolve as ral column immediately. This sort of morphogenetic an adaptation for lightening the skeleton, although it behaviour on the part of diverticula is plausible on the seems to have been exapted for that purpose later in sau- basis of cases in the human clinical literature (e.g. Sadler rischian evolution (Wedel 2003b). et al. 1996; Anorbe et al. 2000). The main argument 218 SPECIAL PAPERS IN PALAEONTOLOGY, 77 against this near-saltational scenario is that the first ver- ticula seem to lie between these extremes. All birds have tebrae to be pneumatized in both sauropodomorphs essentially the same lung architecture; the biggest differ- (Thecodontosaurus, Shunosaurus) and theropods (Coeloph- ence among living forms is the presence or absence of a ysis) are cervicals that are not adjacent to the lungs neopulmo (Duncker 1971). On the other hand, PSP var- (Wedel 2006). ies widely within small clades and even within popula- tions (King 1966; Hogg 1984a; O’Connor 2004). Origin of flow-through ventilation. Flow-through ventila- Diverticula appear to be more conserved than PSP, tion requires that air sacs be present both anterior and although a dedicated study comparing the evolution of posterior to the parenchymal portion of the lung. Given the two is needed. For example, most birds have femoral the pattern of pneumatization found in pterosaurs, sauro- and perirenal diverticula, but the femur and are pods and theropods, we may infer that cervical air sacs only pneumatized in a subset of these taxa (Mu¨ller 1908; were present in the ancestral ornithodiran (or evolved King 1966; Duncker 1971). These observations are neces- independently in pterosaurs and saurischians). The next sarily tentative, given the paucity of phylogenetically problem is to determine when abdominal air sacs origin- based comparative studies of pneumatic diverticula and ated and how many times. PSP (but see O’Connor 2004). Furthermore, our know- In extant birds, the posterior thoracic, synsacral and ledge of variation in the pulmonary system and its diver- caudal vertebrae, pelvic girdle and hindlimb are only ticula is based entirely on extant birds, and may not be pneumatized by diverticula of abdominal air sacs (O’Con- applicable to other saurischians. nor and Claessens 2005; contra Ruben et al. 2003; Chinsa- Nevertheless, the evolutionary malleability of lungs, my and Hillenius 2004; Hillenius and Ruben 2004). So if diverticula and PSP in birds should not be ignored in a fossil is discovered with pneumatic vertebrae reconstructing the pulmonary systems of fossil archosaurs. posterior to the mid-thorax, we have a compelling case The absence of unequivocal PSP in most ‘prosauropods’ for inferring that the had abdominal air sacs. does not mean that they lacked air sacs. Depending on Pneumatic vertebrae in the ‘posterior compartment’ are the preferred phylogenetic hypothesis, Sauropodomorpha present in pterosaurs, diplodocid and macronarian sauro- is only one or two nodes away from . Most pods, and in most clades of neotheropods, but are absent neosauropods have pneumatic vertebrae in the posterior in non-dinosaurian dinosauromorphs, ornithischians, compartment. If these sauropods found some way to herrerasaurids, ‘prosauropods’, basal sauropods, dicraeo- pneumatize the posterior compartment without abdom- saurids, and in basal members of most neotheropod inal air sacs, then surely the same could be true of some clades (e.g. Baryonyx, Ceratosaurus and Allosaurus; pers. or all non-avian theropods. Likewise, if posterior com- obs.). partment pneumaticity is prima facie evidence of abdom- How many times did abdominal air sacs evolve? Poss- inal air sacs in theropods, then abdominal air sacs must ibly just once, before the ornithodiran divergence; poss- also have been present in sauropods (and, by extension, ibly twice, in pterosaurs and saurischians; or possibly pterosaurs). What is good for the goose is good for Gong- three times, in pterosaurs, sauropods and theropods xianosaurus. It is more parsimonious to infer that cervical (Text-fig. 1). We could take this to its logical conclusion and abdominal air sacs were present in the ancestral sau- and assume that abdominal air sacs evolved afresh in rischian, but did not pneumatize the skeleton in ‘prosaur- every group with posterior compartment pneumaticity; opods’, than to infer independent origins of air sacs in this would require the independent origin of abdominal sauropods and theropods. air sacs in ceratosaurs, allosauroids and coelurosaurs, for Most pterosaurs have extensively pneumatized skele- example (not to mention several independent derivations tons, although it is not clear whether pneumaticity is within coelurosaurs). present in any of the forms (Bonde and Chris- The alternative is that some or all of the groups listed tiansen 2003). The presence of PSP in pterosaurs, sau- above had abdominal air sacs but failed to pneumatize ropodomorphs and theropods suggests that air sacs any elements in the posterior compartment. The same may have been present in the ancestral ornithodiran. condition pertains in many extant birds (O’Connor 2004, An apparent problem with pushing the origin of air- table 2). O’Connor and Claessens (2005) posited an ori- sac-driven breathing back before the origin of Sauris- gin of abdominal air sacs by the time of the ceratosaur- chia is the utter absence of PSP in ornithischians. PSP tetanuran divergence, based on the presence of posterior appeared in pterosaurs, sauropodomorphs and thero- compartment pneumatization in Majungatholus, and pods relatively quickly after the divergence of each despite its absence in basal ceratosaurs and basal tetanu- clade: by the in theropods (Colbert 1989) and rans. no later than the Early in pterosaurs and sau- In terms of evolutionary change, ventilation mecha- ropodomorphs (Bonde and Christiansen 2003; Wedel nisms are highly conserved, PSP is highly labile and diver- 2005). If ornithischians had air sacs and diverticula WEDEL: WHAT PNEUMATICITY TELLS US ABOUT ‘PROSAUROPODS’ 219 then it is odd that they never evolved PSP during the bodies, including tracheal dead space, heat retention 160 million of their existence. However, this and oxygen uptake. problem may be more illusory than real. The invasion The one obvious advantage that ‘prosauropods’ did not of bone by pneumatic epithelium is essentially oppor- share with sauropods is the very lightweight skeletal con- tunistic (Witmer 1997). Although pneumatic diverticula struction afforded by pneumaticity. In life, the average may radically remodel both the exterior and the inter- pneumatic sauropod vertebra was approximately 60 per ior of an affected bone, this remodelling cannot occur cent air by volume (Wedel 2005; Woodward 2005; if the diverticula never come into contact with the Schwarz and Fritsch 2006). All else being equal, a sauro- bone, and may not occur even if they do. Furthermore, pod could have a neck two-thirds longer than that of a for all of the potential advantages it conveys, PSP is prosauropod for the same skeletal mass. Pneumaticity still an exaptation of a pre-existing system: in an adap- helped sauropods overcome constraints on neck length, tive sense, lineages that lack PSP do not know what and thereby opened feeding opportunities that were not they are missing. Recall that PSP in basal saurischians available to ‘prosauropods’. How important that differ- did little to lighten the skeleton (see above). Ornithis- ence was is unknown, but it is worth considering in chians may have had air sacs without diverticula, or reconstructions of sauropodomorph evolution and pal- diverticula without PSP. It is pointless to consider the aeobiology. advantages that ornithischians ‘lost’ by never evolving PSP, because that evolution would have hinged on the Acknowledgements. This work was completed as part of a doc- incidental contact of bone and air sac and could not toral dissertation in the Department of Integrative Biology, have been anticipated or sought by natural selection. University of California, Berkeley. I am grateful to my advi- The problem of determining when abdominal air sacs sors, K. Padian and W. A. Clemens, and to the members of evolved is challenging because it forces us to decide my dissertation committee, F. C. Howell, D. Wake and M. Wake, for advice and encouragement. Many thanks to between events of unknown probability: the possibility P. M. Barrett and T. Fedak for organizing the symposium that ornithischians had an air sac system and never ‘dis- that gave rise to this manuscript. I am grateful for the hospi- covered’ PSP (if abdominal air sacs are primitive for tality and patience of curators and collections managers every- Ornithodira), vs. the possibility that a system of cervical where, especially P. Barrett, S. Chapman, R. Schoch, and abdominal air sacs evolved independently in ptero- M. Moser, A. Henrici, M. Lamanna, R. Cifelli, N. Czaplewski saurs and saurischians. Currently, available evidence is and J. Person. L. Claessens, R. Irmis, S. Nesbitt and P. insufficient to falsify either hypothesis. O’Connor provided many inspiring discussions and gracious access to their unpublished work. R. Irmis and M. Taylor Sauropodomorph palaeobiology. It is likely that ‘prosauro- read early drafts of this paper and made many helpful sugges- pods’ had cervical and abdominal air sacs, given the tions, as did my dissertation committee members. L. Claessens strong evidence for both in sauropods and theropods. We and J. Harris provided thoughtful review comments that greatly improved this paper, and I thank them for their time may not be able to determine for certain whether ‘pro- and effort. A translation of Janensch (1947) was made by sauropods’ had a bird-like flow-through lung, but the G. Maier, whose effort is gratefully acknowledged. Funding for requisite air sacs were almost certainly present. Our null this project was provided by the Jurassic Foundation, Sigma hypothesis for the respiratory physiology of ‘prosauro- Xi, the Department of Integrative Biology at the University of pods’ should take into account some form of air-sac-dri- California, Berkeley, the University of California, Museum of ven ventilation. Paleontology, and the UCMP Doris and Samuel P. Welles The air sacs of birds mitigate the problem of tracheal Fund. This is UCMP Contribution no. 1919. dead space (Schmidt-Nielsen 1972), and some birds have improbably long tracheae (i.e. longer than the entire body of the bird; see McClelland 1989). In addi- REFERENCES tion, birds can ventilate their air sacs without blowing air through the lungs, which allows them to avoid alka- ALCOBER, O. and PARRISH, J. M. 1997. 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APPENDIX cent air by volume, based on observations of broken specimens, so the volume of bone removed during pneumatization of the 3 The method of calculating the volumes of bone removed by cervical vertebrae was c. 40 cm ,or0Æ17 per cent of the volume pneumatization in Coelophysis and Thecondontosaurus (see ‘Pal- of the body. aeobiological implications’ above) is provided here. To estimate For Thecondontosaurus caducus it is simpler to calculate the the whole body volumes of the dinosaurs I used graphic double volumes of the individual fossae. The fossae on cervicals 6–8 are integration (GDI: Jerison 1973; Hurlburt 1999; Murray and each c. 5 mm long, 2Æ5 mm tall and 1Æ25 mm deep. The paired Vickers-Rich 2004). I traced over the skeletal reconstructions of fossae on each vertebra can be thought of as forming the two Colbert (1989, fig. 103) and Benton et al. (2000, fig. 19) to make halves of an oblate spheroid with x, y and z diameters of 5, 2Æ5 lateral view body outlines. Dorsal view body outlines were drawn and 2Æ5 mm, respectively. The volume of this spheroid, and thus 3 by hand based on those of Paul (1997) and digitally manipulated the volume of the paired fossae, is 0Æ016 cm . The fossae on to match the dimensions of the skeletal reconstructions. Using cervicals 6–8 are all roughly the same size, and the visible fossa GDI, I obtained whole body volumes of 23Æ5 L for Coelophysis on the ninth cervical is only about half as deep. The volume of 3 and 3Æ3 L for the holotypic individual of Thecodontosaurus cadu- bone removed during fossa formation is therefore 0Æ057 cm ,or cus; the latter animal is a small juvenile. Adjusted for scale, these 0Æ0017 per cent of the volume of the body. results are consistent with previous mass estimates for both taxa These calculations are all approximate, but they are sufficient (Peczkis 1994). to demonstrate that PSP did not have a noticeable effect on the Pneumaticity is present throughout the cervical series of Coel- skeletal mass of basal saurischians. In the case that I have under- ophysis. The total length of the cervical series is c. 50 cm, and estimated the volume of the pneumatic chambers in Coelophysis the vertebral centra have a mean diameter of 1 cm, based on relative to the body volume by a factor of six: the volume of measurements of uncatalogued CM specimens. The neural spines these chambers would still only be 1 per cent of the volume of are roughly the same size as the centra. The combined cervical the body. In contrast, the volume of air in the pneumatic verte- centra are treated as a simple cylinder 50 cm long with a diam- brae of and Diplodocus accounted for 4–6 per eter of 1 cm, which yields a volume of 40 cm3. If the neural cent of the volume of the animals. These air spaces replaced spines are assumed to be equal in volume to the centra, the bone, a relatively dense tissue, and lightened the animals by combined volume of the cervical vertebrae is 80 cm3. The cervi- 7–10 per cent (Wedel 2004, 2005). cal vertebrae of Coelophysis are probably not more than 50 per

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